Terrestrial invasion of pomatiopsid gastropods in the heavy-snow region of the Japanese Archipelago.

Kameda Y, Kato M - BMC Evol. Biol. (2011)

Bottom Line:
Gastropod mollusks are one of the most successful animals that have diversified in the fully terrestrial habitat.Because snow coverage maintains stable temperatures and high humidity on the ground surface, heavy-snow conditions may have paved the way for these organisms from freshwater to land via mountain streamlets by preventing winter desiccation in mountain valleys.The fact that the terrestrialization of Pomatiopsidae occurred only in year-round wet environments, but not in seasonally dried regions, provides new insight into ancient molluscan terrestrialization.

Background: Gastropod mollusks are one of the most successful animals that have diversified in the fully terrestrial habitat. They have evolved terrestrial taxa in more than nine lineages, most of which originated during the Paleozoic or Mesozoic. The rissooidean gastropod family Pomatiopsidae is one of the few groups that have evolved fully terrestrial taxa during the late Cenozoic. The pomatiopsine diversity is particularly high in the Japanese Archipelago and the terrestrial taxa occur only in this region. In this study, we conducted thorough samplings of Japanese pomatiopsid species and performed molecular phylogenetic analyses to explore the patterns of diversification and terrestrial invasion.

Results: Molecular phylogenetic analyses revealed that Japanese Pomatiopsinae derived from multiple colonization of the Eurasian Continent and that subsequent habitat shifts from aquatic to terrestrial life occurred at least twice within two Japanese endemic lineages. Each lineage comprises amphibious and terrestrial species, both of which are confined to the mountains in heavy-snow regions facing the Japan Sea. The estimated divergence time suggested that diversification of these terrestrial lineages started in the Late Miocene, when active orogenesis of the Japanese landmass and establishment of snowy conditions began.

Conclusions: The terrestrial invasion of Japanese Pomatiopsinae occurred at least twice beside the mountain streamlets of heavy-snow regions, which is considered the first case of this event in the area. Because snow coverage maintains stable temperatures and high humidity on the ground surface, heavy-snow conditions may have paved the way for these organisms from freshwater to land via mountain streamlets by preventing winter desiccation in mountain valleys. The fact that the terrestrialization of Pomatiopsidae occurred only in year-round wet environments, but not in seasonally dried regions, provides new insight into ancient molluscan terrestrialization.

Figure 5: Maximum clade probability tree displayed as a chronogram and paleogeography around the Japanese Archipelago. (A) Divergence times calculated in BEAST based on fossil records (outgroups not shown). Japanese pomatiopsid taxa are indicated by asterisks. Horizontal bars in the tree give the 95% credible interval for the age of each node. Numbers above and below branches represent mean node ages and posterior probabilities, respectively. (B, C) Hypothesized paleodistribution of clades I and II. Paleogeographic maps of East Asia were modified from Iijima & Tada [37]. Shaded areas indicate land. (B) Early Miocene (23-18 Ma), divergence of two clades. (C) Middle to late Pliocene (3.5-2 Ma), ongoing diversification and range expansion within each clade.

Mentions:
To determine the timing of the origin of terrestriality in Pomatiopsidae, we estimated the divergence time based on the combined phylogeny of four genes. Fossil records and previous estimations were used to estimate the divergence time of pomatiopsid taxa. For the fossil records, Assiminea spp. from the Lower Miocene (23.0-16.0 Ma) [29,30] were used for the initial divergence of Assimineidae. The root node of "Truncatelloidea" (Truncatellidae + Pomatiopsidae + Assimineidae; sensu Ponder [31]) was modeled by a Gamma prior (shape = 1 and scale = 1.5) with values younger than 61.7 Ma assigned zero probability, which is justified by Truncatella minor, the oldest known fossil for this group documented from the Lower Paleocene (65.5-61.7 Ma) of Belgium [32]. Based on these constraints, a basal split within Triculinae was inferred at 16.8 Ma with a 95% confidence interval of 21.3-12.2 Ma (Figure 5A). The emergence of Japanese aquatic species O. minima and F. ooyagii were estimated at 16.0 (21.2-10.6) Ma and 17.4 (23.7-11.1) Ma, respectively. The terrestrial lineage in clade I began to diverge at 6.4 (9.2-3.7) Ma. The diversification of clade II began at 7.2 (10.3-4.4) Ma and the terrestrial species B. integra occurred during the Pliocene.

Figure 5: Maximum clade probability tree displayed as a chronogram and paleogeography around the Japanese Archipelago. (A) Divergence times calculated in BEAST based on fossil records (outgroups not shown). Japanese pomatiopsid taxa are indicated by asterisks. Horizontal bars in the tree give the 95% credible interval for the age of each node. Numbers above and below branches represent mean node ages and posterior probabilities, respectively. (B, C) Hypothesized paleodistribution of clades I and II. Paleogeographic maps of East Asia were modified from Iijima & Tada [37]. Shaded areas indicate land. (B) Early Miocene (23-18 Ma), divergence of two clades. (C) Middle to late Pliocene (3.5-2 Ma), ongoing diversification and range expansion within each clade.

Mentions:
To determine the timing of the origin of terrestriality in Pomatiopsidae, we estimated the divergence time based on the combined phylogeny of four genes. Fossil records and previous estimations were used to estimate the divergence time of pomatiopsid taxa. For the fossil records, Assiminea spp. from the Lower Miocene (23.0-16.0 Ma) [29,30] were used for the initial divergence of Assimineidae. The root node of "Truncatelloidea" (Truncatellidae + Pomatiopsidae + Assimineidae; sensu Ponder [31]) was modeled by a Gamma prior (shape = 1 and scale = 1.5) with values younger than 61.7 Ma assigned zero probability, which is justified by Truncatella minor, the oldest known fossil for this group documented from the Lower Paleocene (65.5-61.7 Ma) of Belgium [32]. Based on these constraints, a basal split within Triculinae was inferred at 16.8 Ma with a 95% confidence interval of 21.3-12.2 Ma (Figure 5A). The emergence of Japanese aquatic species O. minima and F. ooyagii were estimated at 16.0 (21.2-10.6) Ma and 17.4 (23.7-11.1) Ma, respectively. The terrestrial lineage in clade I began to diverge at 6.4 (9.2-3.7) Ma. The diversification of clade II began at 7.2 (10.3-4.4) Ma and the terrestrial species B. integra occurred during the Pliocene.

Bottom Line:
Gastropod mollusks are one of the most successful animals that have diversified in the fully terrestrial habitat.Because snow coverage maintains stable temperatures and high humidity on the ground surface, heavy-snow conditions may have paved the way for these organisms from freshwater to land via mountain streamlets by preventing winter desiccation in mountain valleys.The fact that the terrestrialization of Pomatiopsidae occurred only in year-round wet environments, but not in seasonally dried regions, provides new insight into ancient molluscan terrestrialization.

Background: Gastropod mollusks are one of the most successful animals that have diversified in the fully terrestrial habitat. They have evolved terrestrial taxa in more than nine lineages, most of which originated during the Paleozoic or Mesozoic. The rissooidean gastropod family Pomatiopsidae is one of the few groups that have evolved fully terrestrial taxa during the late Cenozoic. The pomatiopsine diversity is particularly high in the Japanese Archipelago and the terrestrial taxa occur only in this region. In this study, we conducted thorough samplings of Japanese pomatiopsid species and performed molecular phylogenetic analyses to explore the patterns of diversification and terrestrial invasion.

Results: Molecular phylogenetic analyses revealed that Japanese Pomatiopsinae derived from multiple colonization of the Eurasian Continent and that subsequent habitat shifts from aquatic to terrestrial life occurred at least twice within two Japanese endemic lineages. Each lineage comprises amphibious and terrestrial species, both of which are confined to the mountains in heavy-snow regions facing the Japan Sea. The estimated divergence time suggested that diversification of these terrestrial lineages started in the Late Miocene, when active orogenesis of the Japanese landmass and establishment of snowy conditions began.

Conclusions: The terrestrial invasion of Japanese Pomatiopsinae occurred at least twice beside the mountain streamlets of heavy-snow regions, which is considered the first case of this event in the area. Because snow coverage maintains stable temperatures and high humidity on the ground surface, heavy-snow conditions may have paved the way for these organisms from freshwater to land via mountain streamlets by preventing winter desiccation in mountain valleys. The fact that the terrestrialization of Pomatiopsidae occurred only in year-round wet environments, but not in seasonally dried regions, provides new insight into ancient molluscan terrestrialization.